Exploring the effects of different fertilizer application durations on the functional microbial profiles of soil carbon and nitrogen cycling by using metagenomics in Paulownia plantations in a subtropical zone

Sen Liu1, Xia Li1, Yujia Fu1, Peng Li2, Jie Qiao3, Hui Li4, Lichao Wu1, Baoping Wang3, Sheng Lu1
1Key Laboratory of Cultivation and Protection for Non-Wood Forest Trees, Forestry College, Central South University of Forestry and Technology, Ministry of Education, Changsha, China
2Guangxi Zhuang Autonomous Region Forestry Research Institute, Nanning City, China
3Research Institute of Non-Timber Forestry, Chinese Academy of Forestry, Zhengzhou, China
4Guangxi Diyuanzhiben Fertilizer Industry Co., Ltd., Nanning, China

Tóm tắt

Paulownia fortunei, one of the world’s fastest growing timber tree species, is universally applied with fertilizer as a management approach to meet the nutrient requirements for efficient cultivation. The substantial effects of fertilizer on soil microorganisms in Paulownia plantations have been empirically tested; however, the successive chronosequence of soil microbial carbon and nitrogen functional genes under different fertilizer application durations remains limited. The objective of this study was to explore the characteristics of soil microorganisms involved in carbon and nitrogen cycling and greenhouse gas (GHG) production under different fertilizer application durations. Different fertilizer treatments, i.e., the short-term group (SG) versus the long-term group (LG), and durations were applied to subtropical plantations in southern China and compared with zonal evergreen broad-leaved forests. Results showed that fertilizer treatment significantly increased the relative abundance of Acidobacteriota and the expression of nirK and nosZ. The functional groups that dominated metabolism in SG and LG treatments belonged to Actinobacteria and Acidobacteriota, respectively, suggesting that the nutrient preference of microorganisms in forest soil may change from copiotrophs to oligotrophs with increasing fertilizer application duration. Correlation network analysis showed that the communities that dominated the carbon and nitrogen cycles belonged to Actinobacteria and Acidobacteriota, respectively, and were closely related to ammonium nitrogen and available iron. Actinobacteria and Acidobacteriota were likely the major taxa that affected soil GHG production under different fertilizer application durations. We concluded that long-term fertilizer use changed the preference of microbial nutrient uptake into recalcitrant nutrients, and the sensitivity of the microbial community to nutrients gradually decreased with increasing fertilizer application time. The dominant Actinobacteria affected soil carbon and nitrogen cycles largely by stimulating denitrification to increase the release of nitrous oxide, which might lead to the loss of nitrogen components and the intensification of the GHG effect with increasing fertilizer application time.

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Averill C, Waring B (2018) Nitrogen limitation of decomposition and decay: how can it occur? Glob Chang Biol 24:1417–1427. https://doi.org/10.1111/gcb.13980 Brenzinger K, Drost SM, Korthals G, Bodelier PLE (2018) Organic residue amendments to modulate greenhouse gas emissions from agricultural soils. Front Microbiol 9:3035. https://doi.org/10.3389/fmicb.2018.03035 Deepak Bhardwaj MWA, Ranjan Kumar Sahoo and Narendra Tuteja (2014) Biofertilizers function as key player in sustainable agriculture by improving soil fertility, plant tolerance and crop productivity. Microbial Cell Factories Fierer N, Lauber CL, Ramirez KS, Zaneveld J, Bradford MA, Knight R (2012) Comparative metagenomic, phylogenetic and physiological analyses of soil microbial communities across nitrogen gradients. ISME J 6:1007–1017. https://doi.org/10.1038/ismej.2011.159 Goldberg S, Suarez DL (2014) A new soil test for quantitative measurement of available and adsorbed boron. Soil Sci Soc Am J 78:480–485. https://doi.org/10.2136/sssaj2013.09.0404 Gong H, Du Q, Xie S, Hu W, Akram MA, Hou Q, Dong L, Sun Y, Manan A, Deng Y, Ran J, Deng J (2021) Soil microbial DNA concentration is a powerful indicator for estimating soil microbial biomass C and N across arid and semi-arid regions in northern China. Appl Soil Ecol 160:103869. https://doi.org/10.1016/j.apsoil.2020.103869 Hall JR, Mitchell KR, Jackson-Weaver O, Kooser AS, Cron BR, Crossey LJ, Takacs-Vesbach CD (2008) Molecular characterization of the diversity and distribution of a thermal spring microbial community by using rRNA and metabolic genes. Appl Environ Microbiol 74:4910–4922. https://doi.org/10.1128/AEM.00233-08 Hall EK, Bernhardt ES, Bier RL, Bradford MA, Boot CM, Cotner JB, Del Giorgio PA, Evans SE, Graham EB, Jones SE, Lennon JT, Locey KJ, Nemergut D, Osborne BB, Rocca JD, Schimel JP, Waldrop MP, Wallenstein MD (2018) Understanding how microbiomes influence the systems they inhabit. Nat Microbiol 3:977–982. https://doi.org/10.1038/s41564-018-0201-z Han X, Schubert CJ, Fiskal A, Dubois N, Lever MA (2020) Eutrophication as a driver of microbial community structure in lake sediments. Environ Microbiol 22:3446–3462. https://doi.org/10.1111/1462-2920.15115 Hu X, Liu J, Wei D, Zhu P, Xa C, Zhou B, Chen X, Jin J, Liu X, Wang G (2017) Effects of over 30-year of different fertilization regimes on fungal community compositions in the black soils of northeast China. Agr Ecosyst Environ 248:113–122. https://doi.org/10.1016/j.agee.2017.07.031 Kielak AM, Barreto CC, Kowalchuk GA, van Veen JA, Kuramae EE (2016) The ecology of acidobacteria: moving beyond genes and genomes. Front Microbiol 7:744. https://doi.org/10.3389/fmicb.2016.00744 Kobierski M, Lemanowicz J, Wojewódzki P, Kondratowicz-Maciejewska K (2020) The effect of organic and conventional farming systems with different tillage on soil properties and enzymatic activity. Agronomy 10:1809. https://doi.org/10.3390/agronomy10111809 Kuypers MMM, Marchant HK, Kartal B (2018) The microbial nitrogen-cycling network. Nat Rev Microbiol 16:263–276. https://doi.org/10.1038/nrmicro.2018.9 Liao C, Tian Q, Liu F (2020) Nitrogen availability regulates deep soil priming effect by changing microbial metabolic efficiency in a subtropical forest. J for Res 32:713–723. https://doi.org/10.1007/s11676-020-01148-0 Lin Y, Ye G, Kuzyakov Y, Liu D, Fan J, Ding W (2019) Long-term manure application increases soil organic matter and aggregation, and alters microbial community structure and keystone taxa. Soil Biol Biochem. https://doi.org/10.1016/j.soilbio.2019.03.030 Liu W, Jiang L, Hu S, Li L, Liu L, Wan S (2014) Decoupling of soil microbes and plants with increasing anthropogenic nitrogen inputs in a temperate steppe. Soil Biol Biochem 72:116–122. https://doi.org/10.1016/j.soilbio.2014.01.022 Liu J, Wu L, Chen D, Li M, Wei C (2017) Soil quality assessment of different Camellia oleifera stands in mid-subtropical China. Appl Soil Ecol 113:29–35. https://doi.org/10.1016/j.apsoil.2017.01.010 Moorhead DL, Sinsabaugh RL (2006) A theoretical model of litter decay and microbial interaction. Ecol Monogr 76(2):151–174. https://doi.org/10.2307/27646035 Pan G, Zhou P, Li Z, Smith P, Li L, Qiu D, Zhang X, Xu X, Shen S, Chen X (2009) Combined inorganic/organic fertilization enhances N efficiency and increases rice productivity through organic carbon accumulation in a rice paddy from the Tai Lake region, China. Agr Ecosyst Environ 131:274–280. https://doi.org/10.1016/j.agee.2009.01.020 Pan H, Chen M, Feng H, Wei M, Song F, Lou Y, Cui X, Wang H, Zhuge Y (2020) Organic and inorganic fertilizers respectively drive bacterial and fungal community compositions in a fluvo-aquic soil in northern China. Soil and Tillage Research 198:104540. https://doi.org/10.1016/j.still.2019.104540 Sardans J, Peñuelas J, Ogaya R (2008) Experimental drought reduced acid and alkaline phosphatase activity and increased organic extractable P in soil in a Quercus ilex Mediterranean forest. Eur J Soil Biol 44:509–520. https://doi.org/10.1016/j.ejsobi.2008.09.011 Shrestha RK, Strahm BD, Sucre EB (2014) Greenhouse gas emissions in response to nitrogen fertilization in managed forest ecosystems. New for 46:167–193. https://doi.org/10.1007/s11056-014-9454-4 Siles JA, Cajthaml T, Filipova A, Minerbi S, Margesin R (2017) Altitudinal, seasonal and interannual shifts in microbial communities and chemical composition of soil organic matter in Alpine forest soils. Soil Biol. https://doi.org/10.1016/j.soilbio.2017.04.014 Spohn M, Pötsch EM, Eichorst SA, Woebken D, Wanek W, Richter A (2016) Soil microbial carbon use efficiency and biomass turnover in a long-term fertilization experiment in a temperate grassland. Soil Biol Biochem 97:168–175. https://doi.org/10.1016/j.soilbio.2016.03.008 Staff SS (1999) Soil taxonomy: a basic system of soil classification for making and interpreting soil surveys. US Department of Agriculture, Soil Conservation Service Sun S, Badgley BD (2019) Changes in microbial functional genes within the soil metagenome during forest ecosystem restoration. Soil Biol Biochem 135:163–172. https://doi.org/10.1016/j.soilbio.2019.05.004 Sun S, Li S, Avera BN, Strahm BD, Badgley BD (2017) Soil bacterial and fungal communities show distinct recovery patterns during forest ecosystem restoration. Appl Environ Microbiol. https://doi.org/10.1128/AEM.00966-17 Sun Y, Men M, Xu B, Meng Q, Bello A, Xu X, Huang X (2019) Assessing key microbial communities determining nitrogen transformation in composting of cow manure using illumina high-throughput sequencing. Waste Manag 92:59–67. https://doi.org/10.1016/j.wasman.2019.05.007 Tian J, Dungait JAJ, Lu X, Yang Y, Hartley IP, Zhang W, Mo J, Yu G, Zhou J, Kuzyakov Y (2019) Long-term nitrogen addition modifies microbial composition and functions for slow carbon cycling and increased sequestration in tropical forest soil. Glob Chang Biol 25:3267–3281. https://doi.org/10.1111/gcb.14750 Trivedi P, Delgado-Baquerizo M, Jeffries TC, Trivedi C, Anderson IC, Lai K, McNee M, Flower K, Pal Singh B, Minkey D, Singh BK (2017) Soil aggregation and associated microbial communities modify the impact of agricultural management on carbon content. Environ Microbiol 19:3070–3086. https://doi.org/10.1111/1462-2920.13779 Tu J, Wang B, McGrouther K, Wang H, Ma T, Qiao J, Wu L (2016) Soil quality assessment under different Paulownia fortunei plantations in mid-subtropical China. J Soils Sediments 17:2371–2382. https://doi.org/10.1007/s11368-016-1478-2 Tu J, Qiao J, Zhu Z, Li P, Wu L (2018) Soil bacterial community responses to long-term fertilizer treatments in Paulownia plantations in subtropical China. Appl Soil Ecol 124:317–326. https://doi.org/10.1016/j.apsoil.2017.09.036 Wang J, Xue C, Song Y, Wang L, Huang Q, Shen Q (2016) Wheat and rice growth stages and fertilization regimes alter soil bacterial community structure but not diversity. Front Microbiol 7:1207. https://doi.org/10.3389/fmicb.2016.01207 Wang JY, Ren CJ, Feng XX, Zhang L, Doughty R, Zhao FZ (2020a) Temperature sensitivity of soil carbon decomposition due to shifts in soil extracellular enzymes after afforestation. Geoderma 374:114426. https://doi.org/10.1016/j.geoderma.2020.114426 Wang L, Xiong X, Luo X, Chen W, Wen S, Wang B, Chen C, Huang Q (2020b) Aggregational differentiation of ureolytic microbes in an Ultisol under long-term organic and chemical fertilizations. Sci Total Environ 716:137103. https://doi.org/10.1016/j.scitotenv.2020.137103 Wood SA, Bradford MA, Gilbert JA, McGuire KL, Palm CA, Tully KL, Zhou J, Naeem S, Manning P (2015) Agricultural intensification and the functional capacity of soil microbes on smallholder African farms. J Appl Ecol 52:744–752. https://doi.org/10.1111/1365-2664.12416 Wu L, Wang B, Qiao J, Zhou H, Wen R, Xue J, Li Z (2014) Effects of trunk-extension pruning at different intensities on the growth and trunk form of Paulownia fortunei. For Ecol Manag 327:128–135. https://doi.org/10.1016/j.foreco.2014.05.008 Xia F, Mei K, Xu Y, Zhang C, Dahlgren RA, Zhang M (2020) Response of N2O emission to manure application in field trials of agricultural soils across the globe. Sci Total Environ 733:139390. https://doi.org/10.1016/j.scitotenv.2020.139390 Xiao W, Chen X, Jing X, Zhu B (2018) A meta-analysis of soil extracellular enzyme activities in response to global change. Soil Biol Biochem 123:21–32. https://doi.org/10.1016/j.soilbio.2018.05.001 Xu Y, Du A, Wang Z, Zhu W, Li C, Wu L (2020) Effects of different rotation periods of Eucalyptus plantations on soil physiochemical properties, enzyme activities, microbial biomass and microbial community structure and diversity. For Ecol Manag 456:117683. https://doi.org/10.1016/j.foreco.2019.117683 Xu Y, Ren S, Liang Y, Du A, Li C, Wang Z, Zhu W, Wu L (2021) Soil nutrient supply and tree species drive changes in soil microbial communities during the transformation of a multi-generation Eucalyptus plantation. Appl Soil Ecol 166:103991. https://doi.org/10.1016/j.apsoil.2021.103991 Xun W, Xu Z, Li W, Ren Y, Huang T, Ran W, Wang B, Shen Q, Zhang R (2016) Long-term organic-inorganic fertilization ensures great soil productivity and bacterial diversity after natural-to-agricultural ecosystem conversion. J Microbiol 54:611–617. https://doi.org/10.1007/s12275-016-6143-3 Yang L, Li T, Li F, Lemcoff JH, Cohen S (2008) Fertilization regulates soil enzymatic activity and fertility dynamics in a cucumber field. Sci Hortic 116:21–26. https://doi.org/10.1016/j.scienta.2007.11.001 Yang S, Chen X, Jiang Z, Ding J, Sun X, Xu J (2020) Effects of biochar application on soil organic carbon composition and enzyme activity in paddy soil under water-saving irrigation. Int J Environ Res Public Health 17:333. https://doi.org/10.3390/ijerph17010333 Yoo K, Amundson R, Heimsath AM, Dietrich WE (2006) Spatial patterns of soil organic carbon on hillslopes: Integrating geomorphic processes and the biological C cycle. Geoderma 130:47–65. https://doi.org/10.1016/j.geoderma.2005.01.008 Zaborowska M, Wyszkowska J, Borowik A (2020) Soil microbiome response to contamination with bisphenol A, bisphenol F and bisphenol S. Int J Mol Sci 21:3529. https://doi.org/10.3390/ijms21103529 Zhang J, Li Y, Chang SX, Jiang P, Zhou G, Liu J, Wu J, Shen Z (2013) Understory vegetation management affected greenhouse gas emissions and labile organic carbon pools in an intensively managed Chinese chestnut plantation. Plant Soil 376:363–375. https://doi.org/10.1007/s11104-013-1996-2 Zhang C, Liu G, Xue S, Wang G (2016) Soil bacterial community dynamics reflect changes in plant community and soil properties during the secondary succession of abandoned farmland in the Loess Plateau. Soil Biol Biochem 97:40–49. https://doi.org/10.1016/j.soilbio.2016.02.013 Zhao J, Ni T, Li J, Lu Q, Fang Z, Huang Q, Zhang R, Li R, Shen B, Shen Q (2016) Effects of organic–inorganic compound fertilizer with reduced chemical fertilizer application on crop yields, soil biological activity and bacterial community structure in a rice–wheat cropping system. Appl Soil Ecol 99:1–12. https://doi.org/10.1016/j.apsoil.2015.11.006 Zhao FZ, Bai L, Wang JY, Deng J, Ren CJ, Han XH, Yang GH, Wang J (2019) Change in soil bacterial community during secondary succession depend on plant and soil characteristics. CATENA 173:246–252. https://doi.org/10.1016/j.catena.2018.10.024 Zheng Y, Mei L, Ji Z, He Z (2013) Immediate effects of nitrogen, phosphorus, and potassium amendments on the methanotrophic activity and abundance in a Chinese paddy soil under short-term incubation experiment. J Soils Sediments. https://doi.org/10.1007/s11368-012-0601-2) Zhu L, Tang Y, Weng Y, Huang K, Wang J, Zhao J, Wu L (2021) Effects of burning harvested residues on the archaeal and bacterial communities of Eucalyptus urophylla substituting native vegetation. Appl Soil Ecol 158:103796. https://doi.org/10.1016/j.apsoil.2020.103796